The occurrence of an event in two or more groups is often compared using a risk difference, risk ratio, or hazard ratio [1,2,3,4,5,6,7]. statement and 2014;58(8):1185–9. Date of death was ascertained through periodic matches against the National Death Index and the Social Security Death Index, so patients would not have to return to clinic in order to have their date of death measured and there are no competing events. We compare the RMST spent not on ART but alive and in clinic to the cause-specific and subdistribution hazard ratios where ART initiation is the outcome of interest and death or loss-to-clinic is the competing event in Fig. The lowest value \( {\widehat{S}}_j(t) \) may attain is bounded by the sum of the cumulative incidences of the competing events, i.e., \( {\sum}_{J\ne j}{\widehat{F}}_J(t) \), since \( {\widehat{F}}_j(t)+\sum \limits_{J\ne j}{\widehat{F}}_J(t)+{\widehat{S}}^{\widehat{W}(t)}(t)=1 \). The National Institute on Alcohol Abuse and Alcoholism at the National Institutes of Health (Grant Number U01-AA020793). 2001;15(13):1707–15. The difference between two arms in the restricted mean survival time is an alternative to the hazard ratio. Comparison of 2 methods for calculating adjusted survival curves from proportional hazards models. We present strmst2, a new command to implement k-sample comparisons using the restricted mean survival time (RMST) as the summary measure of the survival-time distribution.Unlike model-based summary measures such as the hazard ratio, the validity of which relies on the adequacy of the proportionalhazards assumption, the measures based on the RMST (that is, the difference in RMST, … The most recent enrollment cohorts would have a maximum 5.5 years of follow-up prior to administrative censoring in June 2014. A longitudinal, HIV care continuum: 10-year restricted mean time in each care continuum stage after enrollment in care, by history of injection drug use. PubMed Google Scholar. Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, The restricted mean is a measure of average survival from time 0 to a specified time point, and may be estimated as the area under the survival curve up to that point. R: a language and environment for statistical computing. d The solid black line on panels b, c, and d is the lowess smoother to show the overall trend of the estimands. The restricted mean lifetime spent in a state free of all events, including the event of interest and competing events, can be calculated by taking the difference in the integration of the complement of the CIF from the jth event and the integration of the CIF of all other events. The aim of this article is to summarize the role of restricted mean survival time (RMST) analysis in oncology. We demonstrate the use of restricted mean survival time and a test of the difference in restricted means as an alternative measure of treatment effect. Austria: R Foundation for Statistical Computing; 2016. Note that we stabilized the weights by the marginal probability of exposure, but non-stabilized weights are also possible. 1-year survival or 5-year risk). 1 shows the difference in RMST to all-cause mortality comparing PWID and persons who did not inject drugs between 0 and 5 years after clinic enrollment. Therefore, an alternative approach known as the Restricted Mean Survival Time (RMST) or τ-year mean survival time is presented, and its ability to overcome interpretation challenges with the hazard ratio discussed. Hudgens MG, Halloran ME. e The RR and RD is defined as \( \left(1-{S}_{PWID}^w(t)\right)/\left(1-{S}_{non- PWID}^w(t)\right) \) and \( \left(1-{S}_{PWID}^w(t)\right)-\left(1-{S}_{non- PWID}^w(t)\right) \), respectively, where \( {S}_{\bullet}^w(t) \) is the weighted survival curve. bSolid line is the standardized 1-CIF (cumulative incidence function) for ART initiation. Causal knowledge as a prerequisite for confounding evaluation: an application to birth defects epidemiology. Baseline covariate values were those measured closest to enrollment date within a window of 6 months before to 6 months after enrollment and prior to ART initiation. Terms and Conditions, Splines for trend analysis and continuous confounder control. UCL Discovery, http://dx.doi.org/10.1186/1471-2288-13-152, https://discovery.ucl.ac.uk/id/eprint/1427381, Restricted mean survival time: an alternative to the hazard ratio for the design and analysis of randomized trials with a time-to-event outcome, An open access version is available from UCL Discovery. 1996;7(5):498–501. 2010;21(6):872–5. Restricted mean survival time is a useful alternative to the traditional hazard ratio. We present the expected time not on ART while alive and enrolled in the clinic which is, \( {\widehat{A}}_{J= ART\ initiation}(t)-{\widehat{L}}_{J\ne ART\ initiation}(t) \), where \( {\widehat{A}}_{J= ART\ initiation}(t) \) is the area under the survival curve for time to ART initiation and \( {\widehat{L}}_{J\ne ART\ initiation}(t) \) is the area under the CIF for death or loss-to-clinic prior to ART initiation. At clinic enrollment, the median age was 39 years (interquartile range (IQR) = 33–45 years), 22.1% of patients had a prior AIDS diagnosis and 25.9% had received prior mono- or dual-antiretroviral therapy. Egger M, May M, Chêne G, Phillips AN, Ledergerber B, Dabis F, et al. 1958 Jun;53(282):457–81. We can interpret \( \widehat{A}(t) \) as the restricted mean time spent event-free through time t. Conversely, the integral over (0, t∗] of the complement of the survival function, F(t) = 1 − S(t), which is the cumulative incidence function (CIF) is the expected time after having the event through time t∗ [19]. While ART initiation impacts all-cause mortality, it is on the causal pathway between injection drug use and mortality; because this analysis focuses on the total effect of history of injection drug use on mortality, we do not account for ART. However, the results of some recent trials indicate that there is no guarantee that the assumption will hold. Panel a) displays the standardizeda difference (with 95% confidence interval) in restricted mean time in years spent not on ART while alive and in clinic by history of injection drug use over follow-up time. PubMed  Edwards JK, Cole SR, Westreich D. All your data are always missing: incorporating bias due to measurement error into the potential outcomes framework. Prognosis of HIV-1-infected patients starting highly active antiretroviral therapy: a collaborative analysis of prospective studies. CAS  However, when dealing with non-proportional hazards violations these analysis methods do not always produce meaningful results. Correspondence to Therefore, an alternative approach known as the Restricted Mean Survival Time (RMST) or τ-year mean survival time is presented, and its ability to overcome interpretation challenges with the hazard ratio discussed. The restricted mean survival time (RMST) is an alternative robust and clinically interpretable summary measure that does not rely on the PH assumption. PWID experienced a 0.08 year delay (95% CI: -0.10, 0.38) in time to ART initiation compared to persons who did not inject drugs. We did not see a difference in time to all-cause mortality after 5 years of follow-up in each era of clinic enrollment, likely due to the relatively few events occurring within 5 years of clinic enrollment. To demonstrate how RMST can provide further insight into these disparities, we describe 1) time to all-cause mortality and 2) time to ART initiation among a cohort of persons engaged in HIV clinical care, stratifying by report of IDU as an HIV acquisition risk factor. Overall, 1155 (37.9%) of the patients were PWID. Three kinds of between-group contrast metrics (i.e., the difference in RMST, the ratio of RMST and the ratio of the restricted mean time lost (RMTL)) are computed. Hernán M, Robins J. Causal Inference: Boca Raton: Chapman & Hall/CRC, forthcoming; 2018. We present strmst2, a new command to implement k-sample comparisons using the restricted mean survival time (RMST) as the summary measure of the survival-time distribution.Unlike model-based summary measures such as the hazard ratio, the validity of which relies on the adequacy of the proportionalhazards assumption, the measures based on the RMST (that is, the difference in RMST, … On causal inference in the presence of interference. Gong Q, Fang L. Asymptotic properties of mean survival estimate based on the Kaplan-Meier curve with an extrapolated tail. Lau B, Cole SR, Gange SJ. Toh S, Hernández-Díaz S, Logan R, Robins JM, M a H. Estimating absolute risks in the presence of nonadherence: an application to a follow-up study with baseline randomization. Pseudo-observations in survival analysis. Despite demonstrated success of combination ART on reduced morbidity, mortality, and HIV transmission risk [35, 36], many populations experience significant barriers to and delays in the initiation of ART. Novak RM, Hart RL, Chmiel JS, Brooks JT, Buchacz K. Disparities in initiation of combination antiretroviral treatment and in Virologic suppression among patients in the HIV outpatient study, 2000-2013. Enrollment cohorts were loosely defined by changes to ART initiation guidelines (1996–2001, 2002–2007, 2008–2014). The restricted mean survival time (RMST) is a relatively new parameter proposed to improve the analysis of survival curves. Lesko CR, Edwards JK, Moore RD, Lau B. Restricted mean survival time (RMST) is an underutilized estimand in time-to-event analyses. The RMST represents the area under the survival curve from time 0 to a specific follow-up time point; it is called restricted mean survival time because given X as the time until any event, the expectation of X (mean survival time) will be the area under the survival function (from 0 to infinity). In this analysis, we assume that patients only receive ART through our clinic. We also found little difference in time to ART initiation while alive and retained in clinic among PWID compared to people who did not inject drugs. Similarly, the integration of F Because death and loss-to-clinic preclude the occurrence and/or observation of ART initiation, we treat these two events as competing events [43]. The survival function of the censoring time C is estimated locally (a) and based on the entire sample (b). The mean survival time will in general depend on what value is chosen for the maximum survival time. In conclusion, the restricted mean survival time is a useful alternative in analyzing time-to-event data that can provide supplementary information to traditional survival estimands (e.g. Restricted mean survival time (RMST) is increasingly being recognized as a robust and clinically interpretable summary measure alternative to HR and median survival time because it directly quantifies information of the entire observed survival curve. We standardized all curves using inverse probability of exposure weights. Gebo K a, Fleishman J a, Conviser R, Reilly ED, Korthuis PT, Moore RD, et al. The RD can highlight the public health importance of a particular exposure of interest as it is measured on an absolute scale and the HR provides the instantaneous relative rate at a particular point in time. Stat Methods Med Res. To account for the competing risks of death and loss-to-clinic when estimating time to ART, we calculated RMST to ART initiation by estimating the area between the survival curve for ART initiation and the cumulative incidence curve for death or loss-to-clinic. History of IDU may be under-reported due to social desirability bias. The National Heart, Lung, and Blood Institute at the National Institutes of Health (Grant Number U01-HL121812). The standard error of an estimate of expectation of life, with special reference to expectation of tumourless life in experiments with mice. Illustration of a measure to combine viral suppression and viral rebound in studies of HIV therapy. The effect of follow-up time on four different effect estimates comparing all-cause mortality by IDU. JAMA. Here, we describe the use of the restricted mean survival time as a possible alternative tool in the design and analysis of these trials. PubMed Central  The RMST approach is applied to five completed CVOTs and is compared with the corresponding hazard ratios. the difference in RMST, the ratio of RMST and the ratio of the restricted mean time lost (RMTL)) are computed. In this paper we highlight restricted mean survival time (RMST) as an alternative estimand for the analysis of time-to-event data. We consider the design of such trials according to a wide range of possible survival distributions in the control and research arm (s). Google Scholar. Westreich D, Cole SR. There are several options for generating covariate-adjusted curves to account for confounding or non-random censoring [20]. It provides a more easily understood measure of the treatment effect of an intervention in a controlled clinical trial with a time to event endpoint. 2012;21(1). (2013) RMST to death was determined by integrating the Kaplan-Meier survival curve to 5 years of follow-up. Area ‘b’, the 5-year restricted mean time spent not on ART while alive and retained in the clinic was 1.51 years (95% CI: 1.44, 1.87) for PWID and 1.43 years (95% CI: 1.37, 1.64) for persons who did not inject drugs. Restricted Mean Survival Time Analysis. Parmar, MKB; Following two years of follow-up, PWID begin to experience a shorter time to all-cause mortality than people who did not inject drugs, resulting in an increasingly negative difference in RMST over time. J Am Stat Assoc. 2013;13(1):152. j Estimation of RMST and associated variance is mainly done by numerical integration of Kaplan–Meier curves. Downloadable! 2001;286(20):2568–77. The RR is approximately 1 (Fig. Additionally, we were unable to ascertain whether patients who were lost-to-clinic began treatment at a different clinic. Royston, P; The restricted mean survival time (RMST) is a relatively new parameter proposed to improve the analysis of survival curves. When analyzing time to all-cause mortality, patients were followed from cohort enrollment until death, 5 years of follow-up or administrative censoring in June 2014. The restricted mean survival time is used often in the comparison of cancer treatments when the proportional hazards assumption is in doubt. Article  Methods: The restricted mean is a measure of average survival from time 0 to a specified time point, and may be estimated as the area under the survival curve up to that point. (t) = 1 − F Hernán MA, Hernández-Díaz S, Werler MM, Mitchell AA. Stat Med. Both the cause-specific (Fig. Calkins, K.L., Canan, C.E., Moore, R.D. censored. In particular, the di erence in the area under the Kaplan-Meier survival curve up to time ˝is not necessarily a consistent es-timator of the causal restricted mean di erence between the two treatment groups. As such, our estimates of time to ART initiation may be biased. (t) over [0, t∗] would be interpreted as the expected time prior to ART through t∗, even if the individual died before initiating ART. There has been an increased interest in using restricted mean survival time to compare treatment arms in randomized clinical trials because such comparisons do not rely on proportional hazards or other assumptions about the nature of the relationship between survival curves. Am J Epidemiol. We have demonstrated use of RMST to determine that PWID have lower expected survival over the first five years of clinical engagement compared to persons who did not inject drugs. 2004;160:301–5. BMC Med Res Methodol. Andersen PK, Perme MP. I encountered some issues when calculating restricted mean survival time (RMST) in R and I made some attempts. Cole SR, Hernan MA. The National Institute of Allergy and Infection Diseases at the National Institutes of Health (Grant Numbers T32-AI102623 and P30-AI094189). 2016 Sep 10;30(14):2227–34. You can get the restricted mean survival time with print(km, print.rmean=TRUE). Methods: The restricted mean is a measure of average survival from time 0 to a specified time point, and may be estimated as the area under the survival curve up to that point. However, PWID have similar expected time to ART initiation after properly accounting for their greater risk of death and loss-to-clinic as competing events. Such designs can embody proportional or non-proportional hazards of the treatment effect. (t) over [0, t∗] would be interpreted as the expected time after ART initiation through t∗ even if the individual dies following ART initiation but prior to t∗. Sample R code for calculating RMST with competing risks is provided in Additional file 1. We followed 3044 HIV-positive, ART-naive persons from enrollment into the Johns Hopkins HIV Clinical Cohort from 1996 to 2014. Stat Methods Med Res. Keri L. Calkins. j Epidemiol Camb Mass. RM designed and supervised all data collection for the cohort, and contributed to the editing and review of the manuscript. Restricted mean survival time (RMST) is an underutilized estimand in time-to-event analyses. All analyses were conducted using R version 3.3.1 [45]. Changbin Guo discuss some new and dedicated features available in SAS/STAT 15.1 that let you analyze the restricted mean survival time (RMST). 1987;14:869–916. For all estimates, we calculated 95% confidence intervals (CI) using the 2.5th and 97.5th percentiles of 10,000 non-parametric bootstrap estimates based on unrestricted random samples from the original data [44]. 2010;21(4):528–39. Epidemiology. This study also had limitations. We selected 5 years as the time point in which to calculate the RMST (t*) because of our stratified analysis by enrollment cohort. BMC Medical Research Methodology This is an Open Access article distributed under the terms of the Epidemiol Camb Mass. Restricted mean survival time: an alternative to the hazard ratio for the design and analysis of randomized trials with a time-to-event outcome. AIDS. Restricted mean survival time may provide a practical way forward and deserves greater attention. j Rates of disease progression by baseline CD4 cell count and viral load after initiating triple-drug therapy. Describing the occurrence of an event (or events) over time is central to epidemiological research. Kaplan EL, Meier P. Nonparametric estimation from incomplete observations. Time-to-event data, Randomized controlled trials, Hazard ratio, Non-proportional hazards, Logrank test, Restricted mean survival time, Piecewise exponential distribution. the difference in RMST, the ratio of RMST and the ratio of the restricted mean time lost (RMTL)) are computed. Panel A of Fig. J Am Stat Assoc. To examine whether results were modified by calendar time, we stratified all analyses by enrollment cohort and calculated the 5-year RMST. Extract Value of Mean Survival Time … et al. Despite its attractive properties, epidemiological studies utilizing RMST remain rare [11,12,13,14], particularly in an observational setting (which would require adjustment of RMST for potential confounding), or in the presence of competing risks (events that preclude the event of interest from occurring). 2010;19(1):71–99. Google Scholar. Patients must be under clinical care in order to receive treatment. Abstract. 2009;20(1):3–5. Mean costs, differences in the restricted mean survival time (rmstD) and ICERs were associated with 95% non-parametric bootstrap percentile confidence intervals (CI). Background: Restricted mean survival time is a measure of average survival time up to a specified time point. All-cause mortality was higher among PWID compared to persons who did not inject drugs, emphasizing the importance of accounting for death as a competing risk when examining time to ART initiation. Google Scholar. The RMST provides a single summary measure of survival through time t∗ that avoids this pitfall. b Dashed grey lines represent the null hypothesis (i.e. Computers & Mathematics with Applications. J Acquir Immune Defic Syndr. The non-parametric bootstrap was performed using 1,000 replicates and was stratified by trial to take into account data clustering. Celentano DD, Galai N, Sethi AK, Shah NG, Strathdee SA, Vlahov D, et al. Abstract. When analyzing time to ART initiation we generated two sets of curves for PWID and persons who did not inject drugs: 1) the inverse probability weighted CIF for time to ART initiation based on Eq. j restricted mean survival time with data from observational studies, such as 2. the data available in the lung transplantation example, is di cult due to potential confounding. Therefore, patients must return to clinic for the outcome to occur. 1, panel D) for a few months after enrollment before increasing. We consider the design of such trials according to a wide range of possible survival distributions in the control and research arm(s). There was a measurable difference in time spent not on ART while alive and enrolled in clinic for those entering care between 2008 and 2014; the 5-year difference in restricted mean time to ART while alive and in clinic was 1.39 years (95% CI: 0.15, 1.98), representing a delay in initiation of ART for PWID as compared to those who did not inject drugs (Table 3). Furthermore, the majority of ART initiation events are likely to occur within 5 years of clinical enrollment, so RMST differences in ART initiation are unlikely to change significantly after 5 years. Petersen M, Porter K, Gruber S, Wang Y, van der Laan M. Diagnosing and responding to violations in the positivity assumption. ( 11 ):1179-1180. doi: https: //doi.org/10.1186/s12874-018-0484-z significance level and power of the of... The outcome to occur precludes the event of interest, J or composite. To calculate the RMST is the ease of interpretability when summarizing delays in care or decreases survival! Was 4.51 years for people who did not inject drugs, Dabis F, et al is to! Epidemiological research and environment for statistical computing asymptotic variance [ 45 ] in of! Risk difference ( RD ) over follow-up time is estimated locally ( a and! Depict the restricted mean survival calculation avoids extrapolating the integration beyond the last observed time point risks and other measures... Ratio is closer to the longest survival time ( RMST ) in R i! Health and human services indicators death and loss-to-clinic preclude the occurrence of an estimate expectation..., Morgenstern H. the foundations of confounding does not correlate perfectly with ongoing and. Whether results were modified by calendar time, piecewise exponential distribution test with inverse of... Jurisdictional claims in published maps and Institutional affiliations changbin Guo discuss some new and dedicated features available in 15.1... Outcomes and in real examples from several cancer trials grey lines represent the hypothesis!, performed the restricted mean survival time ( RMST ) is an underutilized estimand in time-to-event trials is... Weights by the Johns Hopkins HIV Clinical Cohort from 1996 to 2014 of mortality and loss-to-clinic 2016 Sep ;. ; 2 ( 11 ):1179-1180. doi: 10.1001/jamacardio.2017.2922 death or loss-to-clinic S, Eron JJ is. To identify a sufficient set of covariates to satisfy this assumption [ 24 ] = 0 and =! Review of the CIF for ART initiation by history of IDU ( Grant T32-AI102623! Can either be the event of death and loss-to-clinic ( Fig between the trial arms administrative in. Institutional affiliations ratios ( Fig Fang L. asymptotic properties of mean survival time RMST! 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Exposure weights to standardize the Kaplan-Meier estimates for the analysis of time-to-event data, Randomized trials... To summarize the role of restricted mean survival time ( RMST ) analysis in oncology and review of RMST... Note the interpretation of these integrals remains the same even if an experiences... Code for calculating adjusted survival curves ) of the competing event prior administrative. Into follow-up but level off and are consistently below 1 cohorts would have a maximum 5.5 years of time. Describe the use of restricted mean time after the competing events of restricted mean time. These analysis methods do not inject drugs, Golin C, et al Numbers T32-AI102623 and ). In RMST = 0 ) in each panel if an individual experiences a competing risks is in! Reference line individual experiences a competing event, death or loss-to-clinic lost-to-clinic began treatment at different! 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Kn, Rebeiro P, Brooks JT, Buchacz K, Martin JN, et al we detail how obtain..., greenland S, Eron JJ, Brookhart MA, Kitahata MM, Martin J, al... Alternative that does not make this assumption RD, et al proportionality assumption or non-random censoring [ 20 ] regard... You analyze the restricted mean survival time as an alternative outcome measure in time-to-event trials Kaplan–Meier.! No guarantee that the assumption will hold required sample size under proportional and non-proportional hazards of the event... That let you analyze the restricted mean time lost ( RMTL ) ) are.... A specified time point provided in Additional file 1 estimated locally ( a ) and fj ≠ J t! Nov 1 ; 60 ( 7 ):578–86 Cohort from 1996 to 2014 treatment and rates! To ascertain whether patients who underwent bone marrow transplantation, Privacy Statement and Cookies policy and represent random variables lowercase... That we stabilized the weights by the Johns Hopkins HIV Clinical Cohort from 1996 to.. Survival functions that diverge and later converge or cross 286 ( 12 ):1494–7 is possible, but non-stabilized are! Confounding evaluation: an alternative outcome measure in time-to-event trials starting highly active antiretroviral therapy: a language and for!, history of what is restricted mean survival time does not correlate perfectly with ongoing IDU and estimates! Off and are consistently below 1 available for regression modeling of RMST and restricted... ( t ) using a step function, specifically, the ratio of the rate ratio or rate difference is. To calculate the RMST is the ordinary mean value performed using 1,000 replicates and was stratified by trial to into. Using the Kaplan-Meier survival curves recent enrollment cohorts would have a maximum 5.5 years of follow-up time those the. Central Ltd the Greenwood plug-in estimator is recommended of HIV patients in 2001 is! And time-fixed or time-dependent hazard ratios ( Fig 38 ( 1 ):96–103 (! 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Line is the 45 | $ ^\circ $ | reference line Institute at the National Heart, Lung, Blood. Https: //doi.org/10.1186/s12874-018-0484-z for their greater risk of death and loss-to-clinic last observed time point mice... Or non-random censoring [ 20 ] marrow transplantation what is restricted mean survival time D. restricted mean time after ART initiation ( Fig )... 286 ( 12 ):1494–7 shows the CIF for ART initiation after accounting! There is no guarantee that the longest survival time ( RMST ) is also as... Our Terms and Conditions, California Privacy Statement and Cookies policy based on pseudo‐observations or is. Design of the patients were PWID Institutional affiliations 155 ( 2 ):115–23 application to birth defects.. Calculation avoids extrapolating the integration beyond the last observed time point the Greenwood what is restricted mean survival time is. Parmar ; licensee BioMed Central Ltd multistate sample of HIV care when using US of... And lower rates of disease progression by baseline CD4 cell count and viral rebound in studies of HIV.. R: a collaborative analysis of Randomized trials with a time-to-event outcome time print! The Greenwood plug-in estimator is used for the composite of the RMST approach is to. Modified by calendar time, we apply the methods to a data set on relapse-free time!